The workshop took place on ﻿November 9th 2009, at The Davidson Institute of Science Education, Weizmann Institute.

Invited keynote speaker, Prof. Clive G. Jones, of the Cary Institute of Ecosystem Studies, went out of his way to rewrite his lecture into an article format, exclusively published here on ISEES' website.

Out of the desert toward the Promised Land:

Moshe Shachak and the past, present and future of ecosystem engineering

Clive G. Jones

Cary Institute of Ecosystem Studies, PO Box AB, Millbrook, NY, USA

Abstract

This festschrift tribute to Moshe Shachak traces the history of development of ecosystem engineering. The concept came out of the Negev, has gone far beyond the desert, and holds much promise for the future. Moshe has played and will no doubt continue to play a central role. In honor of Moshe, his wife Dahlia, and their children and grandchildren, I loosely apply the metaphor from childhood to adulthood to the development of the ecosystem engineering concept. I interweave Moshe with the past, present and future of the concept, recounting some of the science and some of the sociology of the science.

A Festschrift for Moshe

It is an honor and pleasure to write this tribute to my long time friend and colleague Moshe Shachak. Not a typical scientific paper, it is nevertheless about a scientific concept – ecosystem engineering. The concept came out of the Negev, has gone far beyond the desert, and holds much promise for the future. Moshe has played and will no doubt continue to play a central role in its development.

Moshe and Dahlia have two 2 children, 5 grandchildren, and prospects for great grandchildren. Like all parents they have had great pleasure and periodic anxiety bringing up their children and grandchildren, just as Moshe and I have experienced pleasure and periodic anxiety with the development of ecosystem engineering. So in honor of Moshe, Dahlia and their family I will loosely apply the metaphor from childhood to adulthood to the ecosystem engineering concept, interweaving Moshe with its past, present and future, including some of the science and some of the sociology of the science.

Preconception, Conception, Gestation and Birth

Unlike babies, it is often difficult to date the conception of a scientific idea from its official birthday, the 1994 Oikos paper [1]. While many parents plan for children, there was no planning. Ecosystem engineering grew out of projects and discussions over a long time. There was no single origin and it does not follow a linear trail, but it does begin 27 years ago with trails made by rock-eating snails.

Preconception: Rock-eating snails

In 1983, Moshe came out of the desert to the newly established Institute of Ecosystem Studies, the first of many visits. With his usual infectious enthusiasm he told me a tale of lichens living inside limestone rocks, of circular grooves on the rocks, and of small snails hiding underneath rocks. He said lichenologists assumed the grooves were made by the circular, endolithic lichen colonies. He postulated they were made by snails that ate these lichens. I was intrigued. In those days I studied herbivory and plant defense. I wondered if endolithic lichens needed to defend themselves; after all, they were already protected inside rocks. We planned work for the following year.

Moshe returned carrying snails and rocks with endolithic lichens; portable ecosystems. Simulating dewfall that activated the snails we videotaped them; indeed, they ate rock! Over the next few years we learned much more although our studies on chemical defense led nowhere. There were 3 rock-eating Euchondrus species in the Negev, one restricted to the Ramon crater. To eat the rock the snails used their radulas – rasping tongues with teeth. Alan Solem, then the world expert on snail tongues (he is now sadly deceased), said there was nothing special about their radulas. They broke a lot of teeth, but like other snails, the radula re-grows continuously from the back. Snails fed whenever there was dew on the rocks, about 210 early mornings a year. We estimated that ca. 21 snails m-2 eating nearly 5g snail-1 year-1 consumed and defecated ca. 1000kg rock ha-1 y-1; soil formation equal in magnitude to aeolian dust deposition in the area. Snail feces were deposited under rocks where snails sheltered in the day. Along with crushed limestone, there was about 0.45% undigested nitrogen in the feces that originally came from dust dissolved in dew and taken up by the lichens. The snails transferred ca. 250g nitrogen ha-1 y-1 to the soil. This was ca. 11% of total annual soil nitrogen inputs, ca. 18% of net annual inputs, and at least 27% of the nitrogen annually accumulated by endolithic lichens from dust. The rather bizarre stories in our Science and Nature papers [2, 3] attracted much media attention. Moshe appeared on BBC TV’s ‘Tomorrow’s World’ (February 17, 1995). A comic strip by Bill Tidy in his well-known ‘Grimbledon Down’ series of the time in New Scientist [4] pointed out that given the huge amount of rock turned into feces we should be
thankful snails do not fly!

In writing the papers we struggled to find a larger context. A discarded draft Science paper conclusion referred to other organisms breaking down rock and similar substrates – lichens, other mollusks, plant roots, parrot fish and corals. Perhaps reflecting the dominance of the trophic paradigm and working at the Institute of Ecosystem Studies, both papers were eventually placed into the contexts of consumers and ecosystem effects of species, revealing how contemporary paradigms and scholastic traditions profoundly influence construal of a discovery.

Conception and gestation: Many influences

Unlike babies I cannot readily separate conception from gestation for ecosystem engineering. There were a number of influences. By the late 1980’s I was familiar with and increasingly influenced by Moshe’s thinking – a seamless blend of concepts and empiricism, unconstrained by taxonomic boundaries or where biology begins or ends, and capable of simultaneous thought on multiple time and space scales about superficially unrelated topics that, of course, turn out to be related. From my visits to the Negev from 1987 onwards, I began to gain my own understanding of this desert. There was a certain transparency to what organisms were doing in the ecosystem. Their effects on the physical environment were clear – burrows of isopods, soil mounds of ants and shrubs, mounds and pits of porcupines, crust on the soil and runoff, human-made Limans, and so on.

The consumer context continued to influence our thinking. We published a paper in 1989 with Tom Bianchi entitled “The positive feedback of consumer population density on resource supply” [5]. Some examples in the paper were classic resource-consumer relationships – aggregations of aphids increasing phloem flow, and ungulate herds increasing nutrient cycling rates – others were not; most notably conveyor belt bioturbating polychaetes and burrowing desert isopods that Tom and Moshe respectively studied. This quote from the paper comparing the two is revealing: “In both situations a greater fitness is gained, per capita, ….. due to increases in resource supply, which both result from alteration of the physical environment ….”. The extended physics of organisms was clearly in our thinking.

In 1989, John Lawton, Director of the newly formed Center for Population Biology in the UK, began annual visits to the Institute. Coming from a blend of population, community and ecosystem ecology the 3 of us were aware of the then deep conceptual divide between those focused on species – population and community ecologists – and ecosystem scientists. We talked about how to bridge the divide, coming up with the idea of a Cary Conference on ‘Linking Species and Ecosystems’. Devising the conceptual framework for the conference helped us develop ecosystem engineering.

As we explored ways species could affect ecosystem functioning it was clear that trophic interactions, while obviously important, were not the whole story. What about all the other things species did in ecosystems? Where did rock-eating snails, bioturbating polychaetes, earthworms burrowing, soil crusts and shrub mounds, and a whole host of seemingly similar organismal activities fit in? Were they all the same? If this was not ‘trophic ecology’ what was it? We collected a great many examples, juxtaposing them with new conceptual models. We tracked down related ideas in the literature. We debated for hours as to what to include and how to define it, ending up with “organisms that directly or indirectly modulate the availability of resources (other than themselves) to other species by causing physical state changes in biotic or abiotic materials” [1]. We wanted to use the term ecosystem to reflect the interaction of the living and non-living, and John proposed the term ‘engineering’ which, without really thinking about how others might misconstrue it, we thought was apt. And so ecosystem engineering was conceived, although not yet born.

What caused the concept to crystallize? First, we knew each other well and had had many conversations around the topic before solidifying it. Second, we were all empirically exposed to the phenomenon; John had just completed studies that involved earthworm engineering [6]. Third, we met regularly in a place where new ideas and risk-taking were encouraged, the Institute of Ecosystem Studies. Fourth, we were faced with a larger challenge of providing a conceptual framework for the Cary Conference.

Birth: Somewhat long but not difficult

John presented the ecosystem engineering paper at the Cary Conference in May 1993 [7]; as lead organizer I had to make other presentations. Moshe gave a paper the two of us wrote on isopods and flow chains connecting species, ecosystems and engineering in space and time [8]. His recent paper on ecological networks in the Journal of the Israel Society of Ecology and Environmental Science developed from flow chains. Other presentations focused or touched on ecosystem engineering, although this was only a part of the conference. John and I wrote about the conference [9], as did Steve Carpenter [10]. They were like birth announcements mixed with other family news since ecosystem engineering was not the sole focus. In the interim, our manuscript went off to Oikos, went through review with no hint of controversies to come. Accepted in September 1993, it was published in early 1994 [1].

The conference book came out in early 1995 [11] eventually doing much to help break down the barriers between species and ecosystem perspectives. Some division clearly remains however, and it may explain some of the controversy about ecosystem engineering I will return to later. I think ecosystem engineering has contributed to breaking down the barriers; the concept requires taking both species and ecosystem perspectives.

A Peaceful Infancy with Slow Development

The two years after the Oikos paper were intellectually quiet. The paper began to be cited, although a number of these were self-citations by John Lawton. With his characteristic forceful enthusiasm he was pushing the idea. His active involvement ended in 2000 when he began a new career as the head of the National Environmental Research Council in the UK. Jim Brown gave the paper a supportive boost [12], but also called us to task for trying to classify organismal interactions, an objection often heard later from some ecologists who did not like us breaking organisms into functional pieces such as their engineering versus trophic roles. With Sol Brand, Moshe and I published a paper on snails and isopods, soil formation, erosion and desalinization, continuing our exploration and integration of Negev engineers [13]. Bill Gurney and John Lawton published the first ecosystem engineering modeling paper [14], paving the way for a steadily increasing number of modeling studies to which both Moshe and I have independently contributed. The Oikos paper was reprinted in “Readings in Ecosystem Management” [15], a compendium of previously published papers. This was flattering but perhaps premature. With the exception of work by Moshe and others in the Negev [16], the management ramifications of ecosystem engineering have begun to receive serious attention only relatively recently. During this period we did little to develop the concept; both Moshe and I had many other non-engineering projects.

A Difficult Childhood

In 1997 we published a follow up paper in an Ecology special issue on positive interactions entitled “Positive and negative effects of organisms as physical ecosystem engineers” [17]. The paper somewhat annoyed the special issue editor who was pushing the importance of positive interactions. However, we found the notion that ecosystem engineering just had positive effects to be conceptually and empirically untenable. The outcome-based thinking in many of the special issue papers was at odds with our approach predicting outcomes from process; a tension underlying some of the subsequent debate. We also changed our minds. The 1994 paper excluded creation of living space; now logically, we included it. We also expanded the ideas and generalizations and clarified the concept.

In 1998 Joseph Alper wrote an article in Science about the Ecology paper [18]. He said that Dave Tilman and others “think that after fine-tuning, the concept of ecosystem engineers may be ready to join an elite set of theories, such as natural selection and predator-prey theory, that help explain how species arise and interact”. We thought this was hype, but flattering. It likely served as an irritant to those questioning the value of the concept. The increasing attention was by no means all positive. In 1997, Mary Power called us to task for the intent implied in the word engineer, which we defended [19-21]. She liked the concept but didn’t like the term engineer. In late 2000, a then graduate student of mine working on beaver engineering effects on diversity received a very nasty review from a famous senior ecologist in response to a paper submitted to Ecology. Blasting ecosystem engineering as ‘jargon’, ‘recycled ideas’, and ‘silly’, the reviewer said that he learnt more from Children’s books on beaver in the library than he did from the paper. Published in Oecologia in 2002 [22], this paper now has over 90 citations, is recognized as a classic study on scaling engineering effects on diversity, and has spawned a great many studies on the topic. Also for Ecology, a young researcher (whose identity I protect) submitting an excellent study applying engineering models some time during this period, was told the paper would be accepted only if the author removed ecosystem engineering from the title; the author did so and it was published. In 2002, in an issue of Trends and Ecology and Evolution featuring ecosystem engineering, Reichmann and Seabloom argued that the concept trivialized organism-environment interactions [23]. Andy Wilby, who had worked with Moshe, vigorously defended the general value, pointing out that it was Reichmann and Seabloom who were doing the trivialization [24, 25].

These and other arguments against the concept are captured in the following questions. Don’t all organisms change the environment? Aren’t all organisms therefore ecosystem engineers? If so, isn’t the concept is too broad to be useful? Don’t engineers always have large or large scale impacts? Shouldn’t engineers be limited to species with large effects? Aren’t engineers and keystone species the same? Why do we need the concept? The concept clearly addresses some, but not all, of the ways organisms can change the abiotic environment and the consequences thereof. It encompasses disparate and oft ignored ecological phenomena not addressed by the historical focus of ecology on trophic relations. If it was so familiar, why was there no reference to the phenomena in ecological textbooks of the time? Was it perhaps because formal recognition and study was not considered central to ecological science, despite being obviously important? The 1994 and 1997 papers drew attention to the ubiquity and importance of this process and its consequences, provided an integrative general framework, laid out a question-based research agenda, and gave it a name. My long-delayed, cathartic response to the criticisms, which include the above and more, appeared in 2007 in the first edited book devoted to ecosystem engineering [26].

The negative experiences encountered in writing, seminars and lectures caused me to avoid ecosystem engineering for five years; something I now regret. I published only two other papers on the topic in the period 1998-2002. It was my wife who encouraged me to continue. She gave me a card with a picture of dead fish floating on a river and a caption that said ‘only dead fish go with the flow’. Moshe experienced the same resistance (personal communication); it was one reason why he stopped pushing ecosystem engineering and focused on landscape modulation [27]. He noted that students accepted it – the young are open to new ideas; and that resistance came from: those who don't like ecosystem ecology, and therefore resist linking organisms and ecosystems; those seeing engineering as intentional – Mary Power’s semantic issue [19-21]; and those feeling threatened because they have invested heavily in models that do not include engineering.

In the light of the now widespread acceptance and use of the concept, the difficult childhood of ecosystem engineering is well represented by a famous joke about the 4 stages of scientific acceptance of an idea attributed, in its most recent guise, to J. B. S. Haldane [28]: 1. This is worthless nonsense; 2. This is an interesting but perverse point of view; 3. This is true but quite unimportant; 4. I always said so. While amusing, there are lessons.For young scientists, do not be deterred by skepticism and resistance. For older scientists, if you do not like an idea, be constructive not destructive, and never descend to personal attacks.

The Present: A Vigorous Teenager

Like a teenage growth spurt, from 1996 onwards there was an exponential increase in number of citations to, and publications on the topic of ecosystem engineering – over 150 publications in 2009 for example [29]. The 1994 and 1997 Jones et al. papers are heavily cited, but many scientists have made novel, widely cited contributions [29]. Like a teenager, there has been some fashion following; citing the papers because others cited the papers. Also like a teenager, ecosystem engineering has acquired many friends and acquaintances. Publication in subject areas outside ecology include biodiversity and conservation, evolutionary biology, geoscience, agronomy, civil engineering and many other fields worldwide [29]. Many are now using the concept, helping advance theory and application and preventing sub-disciplinary balkanization.

Like a teenager, ecosystem engineering attended many gatherings. Numerous conferences and special sessions on the topic have occurred or are scheduled. Also like a teenager, ecosystem engineering is networking. From 2004-2008 a National Center for Ecological Analysis and Synthesis Working Group on ecosystem engineering – Moshe was initially involved with the group – pushed modeling and synthesis forward, also editing the first book on ecosystem engineering theory, modeling and application [30]. Today, ecosystem engineering is taught in numerous universities, has many entries in online encyclopedias, and is the subject of articles and books for the general public. It has entered the general consciousness. When I was in the Galapagos not long ago, park guides referred to corals as ecosystem engineers. In France, a 2008 publicity campaign by Suez Environnement called “Making the planet sustainable is the best job on Earth” used the French word for engineer, accompanied by an image of Nature’s archetype animal engineer, the beaver [31].

What notable scientific trends are being followed by this teenager? One is the adoption of ecosystem engineering into Niche Construction Theory – an evolutionary version of ecosystem engineering, although it encompasses more than this [32]. Others include: paleo-ecosystem engineering; modeling; the development of spatial aspects; engineering combined with trophic ecology; and usage in conservation, restoration, and invasive species management. There have also been numerous new case studies, methods development, a lot of synthesis and generalization, and diverse usage in population, community and ecosystem ecology. Moshe has made contributions to many of these areas. No longer ‘a dead fish’, I have aggressively developed my ecosystem engineering work since 2002 [33], although with the exception of a Negev study on crust and shrubs [34] and a conceptual synthesis that includes much of our Negev work [35], Moshe and I have been plowing independent furrows in this field.

The Future: A Promising Adulthood

Ecosystem engineering has a very promising adulthood, although like parents of many young adults, I am not sure exactly what, and young adults have to make their own decisions. I will say some of what I think fruitful. Most research has been on physical engineering. It is plausible that organisms can ‘chemically engineer’ the abiotic environment [1, 36]. However, whether this differs in form or effect from the inevitable abiotic chemical changes caused by organismal mass transfer – phenomena already addressed by extant theories of resource competition and nutrient cycling – is far from clear. Absent a clear distinction and conception, parsimony says extant theory has primacy. I think this is a challenging problem worthy of attention that I am working on. Further development of conceptual frameworks and models can help drive ecosystem engineering toward a powerful predictive theory, as can greater attention to the spatial dimensions. Some of Moshe’s recent work on landscape modulation is relevant here [27], as is some of mine [33]. The Jones et al. 1994 paper [1] referred to humans as “ecosystem engineers par excellence”. Yet there has been no serious attempt to apply ecosystem engineering to understanding human environmental modification; nor are lessons learnt from studying Nature’s engineers being widely used to improve human environmental modification; nor are we yet extensively using Nature’s engineers as environmental management agents. These are clear challenges for the ecological, social and management sciences. Finally like ecosystem engineering a few years ago, niche construction [32] is undergoing a difficult
childhood. I think there is great potential for ecosystem engineering theory to contribute to evolutionary theory.

Out of the Desert toward the Promised Land: Moshe’s Intellectual Legacy

Moshe’s significant contributions to the development of ecosystem engineering have been a constant thread in this paper. Moshe and Dahlia will likely have great grandchildren, but irrespective of such a genetic legacy there is no doubt about his intellectual legacy. Neither I or nor Moshe will see the Promised Land for ecosystem engineering; this is not because we both expect to die soon, but because, unlike people, ideas can go on and develop forever. For his contributions to ecosystem engineering and many other areas of ecology we all owe Moshe Shachak deep appreciation.

Acknowledgements.

This paper is based on an invited keynote presentation at the Moshe Shachak Festschrift Workshop, Moshe, ‘40 years in the desert’, Israel Society of Ecology and Environmental Sciences, Davidson Institute of Science Education, Weizmann Institute of Science, Rehovot, Israel, November 9, 2009. I thank organizers Marcelo Sternberg and Avi Perevolotsky for the opportunity; the Israel Society of Ecology and Environmental Sciences and Yad Hanadev for travel support; and the Cary Institute of Ecosystem Studies for financial support of my time. This paper is a contribution to the program of the Cary Institute of Ecosystem Studies.